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In Situ Response of Antarctic Under-Ice Primary Producers to Experimentally Altered Ph Received: 3 August 2018 Vonda J

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In Situ Response of Antarctic Under-Ice Primary Producers to Experimentally Altered Ph Received: 3 August 2018 Vonda J www.nature.com/scientificreports OPEN In situ response of Antarctic under-ice primary producers to experimentally altered pH Received: 3 August 2018 Vonda J. Cummings1, Neill G. Barr1, Rod G. Budd2, Peter M. Marriott1, Karl A. Saf2 & Accepted: 29 March 2019 Andrew M. Lohrer2 Published: xx xx xxxx Elevated atmospheric CO2 concentrations are contributing to ocean acidifcation (reduced seawater pH and carbonate concentrations), with potentially major ramifcations for marine ecosystems and their functioning. Using a novel in situ experiment we examined impacts of reduced seawater pH on Antarctic sea ice-associated microalgal communities, key primary producers and contributors to food webs. pH levels projected for the following decades-to-end of century (7.86, 7.75, 7.61), and ambient levels (7.99), were maintained for 15 d in under-ice incubation chambers. Light, temperature and dissolved oxygen within the chambers were logged to track diurnal variation, with pH, O2, salinity and nutrients assessed daily. Uptake of CO2 occurred in all treatments, with pH levels signifcantly elevated in the two extreme treatments. At the lowest pH, despite the utilisation of CO2 by the productive microalgae, pH did not return to ambient levels and carbonate saturation states remained low; a potential concern for organisms utilising this under-ice habitat. However, microalgal community biomass and composition were not signifcantly afected and only modest productivity increases were noted, suggesting subtle or slightly positive efects on under-ice algae. This in situ information enables assessment of the infuence of future ocean acidifcation on under-ice community characteristics in a key coastal Antarctic habitat. Physical and biogeochemical changes in the world’s oceans associated with anthropogenic greenhouse gas emis- sions have potential to impact marine organisms and ecosystems1,2. Ocean acidifcation, the decline in seawater pH (and concomitant decline in carbonate saturation state) as the oceans absorb more CO2, is anticipated to afect organism function3 and alter marine food web dynamics (e.g.4). Oceanic pH is predicted to decline by −0.33 pH units by 2090–2099 (relative to 1990–1999 levels) under the current trajectory of the “business as usual” Representative Concentration Pathway emissions scenario (RCP8.5)5. Tis represents a considerably faster rate of change, and lower pH, than at any time in the last 25 million years6, raising questions of how organisms, pop- ulations and communities will respond to this potential challenge that, in some cases, may transcend adaptation capacity time scales. Te threat of ocean acidifcation is particularly great in cold water environments, where CO2 is absorbed 7,8 more readily and calcium carbonate minerals are more soluble . Absorption of CO2 is occurring more quickly in the Southern Ocean than in subtropical oceans, and its water chemistry is changing at a higher rate than previously predicted9. Tat such high latitude regions will experience early ocean acidifcation, altering benthic and pelagic ecosystems, is a high confdence statement in the most recent Intergovernmental Panel on Climate Change report10. Seasonally undersaturated carbonate conditions, predicted for the Southern Ocean in the com- ing decades (i.e. by 2030 in winter months in the Ross Sea11; and by austral summer of 2026–2030 in the Ross Sea, Amundsen Sea and coastal Amundsen Sea12), will also spread rapidly in aerial extent and temporal duration - 9 particularly from 2040 onwards when atmospheric CO2 is around 450–500 μatm . Antarctic sea ice supports a diverse community of primary producers and consumers, and represents an important multi-trophic module within the broader marine ecosystem13. Sea ice-associated microalgal commu- nities contribute signifcantly to seasonal production13, with estimates of 10–50% of the annual production of polar seas14 and as much as 55–65% in ice covered coastal ecosystems15. Under-ice algal assemblages are an important food resource, not only to organisms utilising the under-side of the ice, but also to the benthos below, as ice algae and detritus sink down to the seafoor, seeding microphytobenthic communities and providing a 1National institute of Water and Atmospheric Research, Wellington, New Zealand. 2National institute of Water and Atmospheric Research, Hamilton, New Zealand. Correspondence and requests for materials should be addressed to V.J.C. (email: [email protected]) SCIENTIFIC REPORTS | (2019) 9:6069 | https://doi.org/10.1038/s41598-019-42329-0 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Infow Outfow Treatment pHT pCO2 DIC ΩAr ΩCa pHT pCO2 DIC ΩAr ΩCa Ambient 7.99 ± 0.002 457.3 ± 7.37 2259.3 ± 2.62 1.2 ± 0.02 1.8 ± 0.03 8.08 ± 0.002 374.9 ± 18.01 2232.4 ± 8.06 1.4 ± 0.05 2.2 ± 0.08 pH low 1 7.86 ± 0.006 641.5 ± 16.28 2301.3 ± 4.48 0.9 ± 0.02 1.4 ± 0.03 8.00 ± 0.005 449.6 ± 25.98 2256.7 ± 8.96 1.2 ± 0.05 1.9 ± 0.09 pH low 2 7.75 ± 0.008 802.3 ± 20.02 2328.0 ± 3.49 0.7 ± 0.02 1.1 ± 0.03 7.96 ± 0.011 504.9 ± 62.24 2269.8 ± 16.73 1.1 ± 0.11 1.7 ± 0.17 pH low 3 7.61 ± 0.006 1166.2 ± 57.47 2373.2 ± 6.97 0.5 ± 0.02 0.8 ± 0.04 7.87 ± 0.012 639.9 ± 90.00 2298.6 ± 18.38 0.9 ± 0.10 1.4 ± 0.16 Table 1. Seawater conditions over the experiment (averages ± SE). Infow = water delivered to the chambers; Outfow = water resident in the chambers for approximately 12 h. Measured pHT is presented at average in situ temperature (−1.85 °C), and is an average over the 14 days of the experiment (N = 14). pCO2 (μatm), dissolved −1 inorganic carbon (DIC; μmol kg ) and saturation states of aragonite and calcite (ΩAr and ΩCa) were calculated using measured pHT, AT, temperature and salinity, and Mehrbach equilibrium constants reft by Dickson and Millero (1987). Tese calculations were done separately for Days 1, 7 and 14, and the averages ( ± SE) of these three days are presented here. Measured AT = 2348.9 ± 1.86, 2344.5 ± 0.636, and 2342.8 ± 6.4, on Days 1, 7 and 14, respectively (N = 14 chambers/day). major food component for benthic primary consumers16–18. In consuming this material, the benthos regenerate nutrients to the water column which, in turn, become available for use by the sea ice communities above (e.g.19). Consequently, impacts on such primary producers could have considerable ramifcations, not least due to their role in carbon cycling. In the Ross Sea, coastal sea ice algal communities are dominated by diatoms. Studies of open ocean phyto- plankton have noted changes to diatom communities under ocean acidifcation conditions projected for the end of this century20. Tese include selection for larger species (e.g.21,22) and, in Southern Ocean waters, alterations in community size structure and nutrient cycling23, and increased growth rates24 particularly of larger diatom 25 species . Investigations of the response of sea ice associated communities or species to elevated pCO2 concen- trations are, however, rare26. McMinn26 identifed three published studies that used temperatures realistic for a sea ice environment (≤0 °C)27–29, and concluded that the general response across studies was either a neutral or positive efect on photosynthesis and/or growth. Additionally, a study of single diatom species (Nitzschia lecointei) in the laboratory showed reduced fatty acid content (indicative of lower food quality) at −1.8 °C and at 960 μatm 28 pCO2 relative to the ambient pCO2 treatment (390 μatm) . Experiments on surface dinofagellate dominated microalgal brine communities within the sea ice in situ found a positive efect at pH below 7.5, on growth27 and photosynthesis30. Given the prevalence of diatom-dominated ice algae communities in the coastal Ross Sea, their exceedingly high concentrations in spring/early summer (up to 1000 μg L−1;31), and the fact that algal photosynthesis is a major contributor to pH variation and carbonate saturation state (e.g.12,32,33), we expect these communities to play a signifcant role in carbon uptake and, potentially, in seasonal mitigation of ocean acidifcation conditions in a high CO2 world. Understanding how ocean acidifcation might afect such processes, and their potential to infuence food and nutrient availability in nearby benthic and pelagic ecosystems, was the impetus behind this in situ experimental study. We describe the results of a pH manipulation experiment conducted at Granite Harbour (Ross Sea), that enclosed relatively large patches (0.36 m2) of natural sea ice-associated (sympagic) microbial community in cham- bers deployed to the underside of the sea ice34. Seawater was introduced to the chambers at ambient pH levels (7.99), and a range of pH levels expected over the following decades-to end of century (7.86, 7.75, 7.61), equiva- lent to average pCO2 concentrations of 457, 642, 802, and 1166 μatm respectively (Table 1). Fluxes of oxygen and nutrients, along with changes in pH, were assessed daily throughout the experimental period (15 d). At the end of the experiment, comparisons of characteristics of the community associated with the bottom and platelet ice were made between treatments. Continuous measurements of photosynthetically available radiation (PAR) and tem- perature inside each chamber were taken into account when analysing and interpreting the results. Specifcally, we asked how exposure to future projected levels of seawater pH modifed sea ice community characteristics and net community primary productivity. Consideration of these efects is key to better understanding consequences of ocean acidifcation on the functioning of sea ice-associated communities, the potential downstream impacts upon other components of coastal ecosystems, and the mediation of seawater CO2 concentrations by seasonal biological uptake and fxation.
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